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Jasmonate-mediated wound signalling promotes plant regeneration

Nature Plants volume 5, pages 491–497 (2019)Cite this article

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Abstract

Wounding is the first event triggering regeneration1,2,3,4. However, the molecular basis of wound signalling pathways in plant regeneration is largely unclear. We previously established a method to study de novo root regeneration (DNRR) in Arabidopsis thaliana5,6, which provides a platform for analysing wounding. During DNRR, auxin is biosynthesized after leaf detachment and promotes cell fate transition to form the root primordium5,6,7. Here, we show that jasmonates (JAs) serve as a wound signal during DNRR. Within 2 h of leaf detachment, JA is produced in leaf explants and activates ETHYLENE RESPONSE FACTOR109 (ERF109). ERF109 upregulates ANTHRANILATE SYNTHASE α1 (ASA1)—a tryptophan biosynthesis gene in the auxin production pathway8,9,10—dependent on the pre-deposition of SET DOMAIN GROUP8 (SDG8)-mediated histone H3 lysine 36 trimethylation (H3K36me3)11 on the ASA1 locus. After 2 h, ERF109 activity is inhibited by direct interaction with JASMONATE-ZIM-DOMAIN (JAZ) proteins to prevent hypersensitivity to wounding. Our results suggest that a dynamic JA wave cooperates with histone methylation to upregulate a pulse of auxin production and promote DNRR in response to wounding.

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Fig. 1: JA serves as a wound signal to promote DNRR.
Fig. 2: JA-ERF109-ASA1 wound signalling pathway in DNRR.
Fig. 3: SDG8-mediated H3K36me3 is involved in wound response.
Fig. 4: Prevention of hypersensitivity to JA-mediated wound signalling.

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Data availability

The data that support the findings of this study are available from the corresponding author upon request.

References

  1. Chen, L., Sun, B., Xu, L. & Liu, W. Wound signaling: the missing link in plant regeneration. Plant Signal. Behav. 11, e1238548 (2016).

    Article  Google Scholar 

  2. Ikeuchi, M. et al. Wounding triggers callus formation via dynamic hormonal and transcriptional changes. Plant Physiol. 175, 1158–1174 (2017).

    Article  CAS  Google Scholar 

  3. Birnbaum, K. D. & Sanchez Alvarado, A. Slicing across kingdoms: regeneration in plants and animals. Cell 132, 697–710 (2008).

    Article  CAS  Google Scholar 

  4. Xu, L. & Huang, H. Genetic and epigenetic controls of plant regeneration. Curr. Top. Dev. Biol. 108, 1–33 (2014).

    Article  Google Scholar 

  5. Liu, J. et al. WOX11 and 12 are involved in the first-step cell fate transition during de novo root organogenesis in Arabidopsis. Plant Cell 26, 1081–1093 (2014).

    Article  CAS  Google Scholar 

  6. Xu, L. De novo root regeneration from leaf explants: wounding, auxin, and cell fate transition. Curr. Opin. Plant Biol. 41, 39–45 (2018).

    Article  CAS  Google Scholar 

  7. Chen, L. et al. YUCCA-mediated auxin biogenesis is required for cell fate transition occurring during de novo root organogenesis in Arabidopsis. J. Exp. Bot. 67, 4273–4284 (2016).

    Article  CAS  Google Scholar 

  8. Niyogi, K. K. & Fink, G. R. Two anthranilate synthase genes in Arabidopsis: defense-related regulation of the tryptophan pathway. Plant Cell 4, 721–733 (1992).

    Article  CAS  Google Scholar 

  9. Sun, J. et al. Arabidopsis ASA1 is important for jasmonate-mediated regulation of auxin biosynthesis and transport during lateral root formation. Plant Cell 21, 1495–1511 (2009).

    Article  CAS  Google Scholar 

  10. Cai, X. T. et al. Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat. Commun. 5, 5833 (2014).

    Article  CAS  Google Scholar 

  11. Zhao, Z., Yu, Y., Meyer, D., Wu, C. & Shen, W. H. Prevention of early flowering by expression of FLOWERING LOCUS C requires methylation of histone H3 K36. Nat. Cell Biol. 7, 1256–1260 (2005).

    Article  Google Scholar 

  12. Da Costa, C. T. et al. When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front. Plant Sci. 4, 133 (2013).

    Article  Google Scholar 

  13. Druege, U., Franken, P. & Hajirezaei, M. R. Plant hormone homeostasis, signaling, and function during adventitious root formation in cuttings. Front. Plant Sci. 7, 381 (2016).

    Article  Google Scholar 

  14. Ahkami, A. H. et al. Molecular physiology of adventitious root formation in Petunia hybrida cuttings: involvement of wound response and primary metabolism. New Phytol. 181, 613–625 (2009).

    Article  CAS  Google Scholar 

  15. Fattorini, L. et al. Adventitious rooting is enhanced by methyl jasmonate in tobacco thin cell layers. Planta 231, 155–168 (2009).

    Article  CAS  Google Scholar 

  16. Lischweski, S., Muchow, A., Guthorl, D. & Hause, B. Jasmonates act positively in adventitious root formation in petunia cuttings. BMC Plant Biol. 15, 229 (2015).

    Article  Google Scholar 

  17. Monte, I. et al. Rational design of a ligand-based antagonist of jasmonate perception. Nat. Chem. Biol. 10, 671–676 (2014).

    Article  CAS  Google Scholar 

  18. Wang, Z. et al. Identification and characterization of COI1-dependent transcription factor genes involved in JA-mediated response to wounding in Arabidopsis plants. Plant Cell Rep. 27, 125–135 (2008).

    Article  CAS  Google Scholar 

  19. Berr, A. et al. Arabidopsis histone methyltransferase SET DOMAIN GROUP8 mediates induction of the jasmonate/ethylene pathway genes in plant defense response to necrotrophic fungi. Plant Physiol. 154, 1403–1414 (2010).

    Article  CAS  Google Scholar 

  20. Li, Y. et al. The histone methyltransferase SDG8 mediates the epigenetic modification of light and carbon responsive genes in plants. Genome Biol. 16, 79 (2015).

    Article  Google Scholar 

  21. Thines, B. et al. JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signalling. Nature 448, 661–665 (2007).

    Article  CAS  Google Scholar 

  22. Chini, A. et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666–671 (2007).

    Article  CAS  Google Scholar 

  23. Kazan, K. & Manners, J. M. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 17, 22–31 (2012).

    Article  CAS  Google Scholar 

  24. Bahieldin, A. et al. Multifunctional activities of ERF109 as affected by salt stress in Arabidopsis. Sci. Rep. 8, 6403 (2018).

    Article  Google Scholar 

  25. Bahieldin, A. et al. Ethylene responsive transcription factor ERF109 retards PCD and improves salt tolerance in plant. BMC Plant Biol. 16, 216 (2016).

    Article  Google Scholar 

  26. Kong, X. et al. PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep. 22, 1350–1363 (2018).

    Article  CAS  Google Scholar 

  27. Gutierrez, L. et al. Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24, 2515–2527 (2012).

    Article  CAS  Google Scholar 

  28. Xu, L. et al. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919–1935 (2002).

    Article  CAS  Google Scholar 

  29. Yang, L. et al. Pseudomonas syringae type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microb. 21, 156–168 (2017).

    Article  CAS  Google Scholar 

  30. Murashige, T. & Skoog, F. A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 80, 662–668 (1962).

    Google Scholar 

  31. Chen, X. et al. A simple method suitable to study de novo root organogenesis. Front. Plant Sci. 5, 208 (2014).

    Article  Google Scholar 

  32. Gamborg, O. L., Miller, R. A. & Ojima, K. Nutrient requirements of suspension cultures of soybean root cells. Exp. Cell Res. 50, 151–158 (1968).

    Article  CAS  Google Scholar 

  33. Mao, Y. B. et al. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nat. Commun. 8, 13925 (2017).

    Article  CAS  Google Scholar 

  34. Sun, L.-J. et al. Electrochemical mapping of indole-3-acetic acid and salicylic acid in whole pea seedlings under normal conditions and salinity. Sens. Actuators B Chem. 276, 543–551 (2018).

    Google Scholar 

  35. Sun, L.-J. et al. Paper-based analytical devices for direct electrochemical detection of free IAA and SA in plant samples with the weight of several milligrams. Sens. Actuators B Chem. 247, 336–342 (2017).

    Article  CAS  Google Scholar 

  36. He, C., Chen, X., Huang, H. & Xu, L. Reprogramming of H3K27me3 is critical for acquisition of pluripotency from cultured Arabidopsis tissues. PLoS Genet. 8, e1002911 (2012).

    Article  CAS  Google Scholar 

  37. Li, G. et al. ISWI chromatin remodeling factors and their interacting RINGLET proteins act together in controlling the plant vegetative phase in Arabidopsis. Plant J. 72, 261–270 (2012).

    Article  CAS  Google Scholar 

  38. Xu, L. et al. Di- and tri- but not monomethylation on histone H3 lysine 36 marks active transcription of genes involved in flowering time regulation and other processes in Arabidopsis thaliana. Mol. Cell Biol. 28, 1348–1360 (2008).

    Article  CAS  Google Scholar 

  39. Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).

    Article  CAS  Google Scholar 

  40. Langmead, B., Trapnell, C., Pop, M. & Salzberg, S. L. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).

    Article  Google Scholar 

  41. Dobin, A. et al. STAR: ultrafast universal RNA-Seq aligner. Bioinformatics 29, 15–21 (2013).

    Article  CAS  Google Scholar 

  42. Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12, 323 (2011).

    Article  CAS  Google Scholar 

  43. Kumar, L. & M, E. F. Mfuzz: a software package for soft clustering of microarray data. Bioinformation 2, 5–7 (2007).

    Article  Google Scholar 

  44. Leng, N. et al. EBSeq: an empirical Bayes hierarchical model for inference in RNA-Seq experiments. Bioinformatics 29, 1035–1043 (2013).

    Article  CAS  Google Scholar 

  45. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).

    Article  Google Scholar 

  46. Stark, R. & Brown, G. DiffBind: differential binding analysis of ChIP-Seq peak data (Cancer Research UK, 2018).

  47. Thorvaldsdottir, H., Robinson, J. T. & Mesirov, J. P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 14, 178–192 (2013).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank the ABRC, Z. Zhu, G. A. Howe and D. Xie for providing the Arabidopsis seeds, Z. Zhu and W. Zhou for helpful discussion, Y. Liu from the Core Facility Centre of SIPPE for technical assistance on JA detection, and J. Pan and D. Cai for help on auxin concentration analysis. This work was supported by grants from the National Natural Science Foundation of China (31630007, 31770399 and 21375066), Strategic Priority Research Program of CAS (grant number XDB27030103), Key Research Program of CAS (QYZDB-SSW-SMC010), Youth Innovation Promotion Association of CAS (2014241 and 2014230) and National Key Laboratory of Plant Molecular Genetics.

Author information

Author notes

  1. Lyuqin Chen

    Present address: Department of Neurosurgery, Stanford University School of Medicine, Stanford, CA, USA

  2. Lyuqin Chen

    Present address: Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, CA, USA

  3. These authors contributed equally: Guifang Zhang, Fei Zhao, Lyuqin Chen.

Authors and Affiliations

  1. National Key Laboratory of Plant Molecular Genetics, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China

    Guifang Zhang, Fei Zhao, Lyuqin Chen, Teng Zhang, Yijing Zhang & Lin Xu

  2. University of Chinese Academy of Sciences, Beijing, China

    Guifang Zhang, Fei Zhao, Lyuqin Chen, Teng Zhang & Chun-Xiao Cui

  3. School of Life Sciences, Nantong University, Nantong, China

    Yu Pan & Lijun Sun

  4. School of Public Health, Nantong University, Nantong, China

    Ning Bao

  5. Shanghai-Hong Kong Joint Laboratory in Chemical Synthesis, Shanghai Institute of Organic Chemistry, Chinese Academy of Sciences, Shanghai, China

    Chun-Xiao Cui & Zaozao Qiu

  6. Department of Plant Pathology, University of Georgia, Athens, GA, USA

    Li Yang

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Contributions

G.Z., L.C. and L.X. designed the research. G.Z., F.Z. and Y.Z. performed the RNA-seq and ChIP-seq analyses. G.Z., Y.P., L.S. and N.B. analysed the auxin concentration. C.-X.C. and Z.Q. synthesized the COR-MO. L.Y. performed the Co-IP. G.Z., L.C. and T.Z performed the other experiments. G.Z., F.Z., L.Y. and L.X. analysed the data. L.X. wrote the article.

Corresponding author

Correspondence to Lin Xu.

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The authors declare no competing interests.

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Journal peer review information: Nature Plants thanks Jian Xu and the other anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figures 1–7 and Supplementary Table 2.

Reporting Summary

Supplementary Table 1

List of cluster-1 to -10 genes and JA- and auxin-related genes.

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Cite this article

Zhang, G., Zhao, F., Chen, L. et al. Jasmonate-mediated wound signalling promotes plant regeneration. Nat. Plants 5, 491–497 (2019). https://doi.org/10.1038/s41477-019-0408-x

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